Gigantism in Insects

There are several ecological and evolutionary patterns concerning body size. One of the most observeable ones, consistent among everything from bacteria to plants and animals is the temperature-size rule: species in colder environments tend to be larger, as are members of a population of the same species living in cold environments (Ashton, 2004); the latter is referred to as Bergmann’s Rule. They’re both enabled by phenotypic plasticity (Atkinson, 1995).

Another trend is the island rule, a term coined by Van Valen (1973), based on the formalisation by Foster (1964), itself based on the the proposal by Nopsca (1914), which in turn was based on observations by palaeontologists working on Mediterranean island mammals, e.g. Bate (1903). It states that small animals isolated on islands become bigger (island gigantism), while large animals become smaller (island dwarfism). The causal basis of this rule is mainly resource availability (McNab, 1999): originally large mammals will not find enough food to sustain their sizes, so smaller individuals will be selected for, while originally small mammals can reach larger sizes due to an abundance of food with lack of competition.

A look at the papers cited above in support of these rules reveals a very strong bias towards vertebrates. The insects of today are renowned for their miniaturisation, with the bulk of insect biodiversity lying in mm-sized beetles, hymenopterans and flies, with the average size of adult beetles being 4-5 mm (Mound & Waloff, 1978); the smallest insect known so far is the mymarid wasp Dicopomorpha echmepterygis, the male of which is ~139 µm large.

There have been several hypotheses proposed as to why insects are so small. Ecological possibilities include predation pressure from larger vertebrates keeping them small (Damuth, 1981). Biomechanical possibilities include the non-scalability of exoskeletons (Price, 1997). While both of these have undoubteably played some factor, it is oxygen levels that have been presumed to have played the largest role (Dudley, 1998). This idea can be tested using the fossil record – there were times in Earth’s history when the oxygen levels were higher than today. If the hypothesis is valid, then the insects of the time should be larger.

Back in the Carboniferous and Permian, insects were subject to gigantism, due to an atmosphere that was very high in oxygen (Graham et al., 1995) – they peaked at 35% at the Carboniferous-Permian boundary compared to today’s 21% (Berner & Canfield, 1989); see the diagram above (Dudley, 2000). It was in this time that the 70 cm large Protodonata pictured in this post lived.

Three orders of Palaeozoic insect, all of which went extinct in the end-Permian mass extinction, were particularly affected by gigantism: the Megasecoptera, the Palaeodictyoptera, and the Protodonata; and some members of other orders, for example the Ephemeroptera (45 cm wingspan mayflies!) and Meganeuridae, also had gigantic forms (Shear & Kukalová-Peck, 1990). It’s also important to note that not all insects back then were gigantic though, the majority were regular-sized.

As more evidence of oxygen’s role, we know that these gigantic forms went extinct as oxygen levels declined drastically in the Permian (Huey & Ward, 2005), and some gigantic forms re-evolved in the Cretaceous oxygen peak (Dudley, 2000).

We can speculate a bit about how these animals flew. One thing is clear: they had enough biomass to be able to support them, since the climates were tropical, with all-year-round growth. They might have had a much easier time getting off the ground, as the air density would have been higher, making lift production much easier (that is, if we assume that nitrogen and trace element partial pressures were similar to today’s level). What is definitely known is that these gigantic insects were putting their wings to good use – like modern odonates, the gigantic Palaeozoic insects also had plenty of veins in their wings, meaning they needed them to be strong and flexible, so they were actively hunting (or evading predators?) in mid-air. The high oxygen levels would have helped on the physiological level too: insect flight is an extremely oxygen-consuming effort, with oxygen consumption rising 100-fold, so having more oxygen in the atmosphere means that insects can fly longer without their muscles getting deprived of oxygen (Harrison et al., 2006). This is especially important for those insects that depend on their wing muscles instead of the thorax’s contraction for moving the wings, e.g. odonates. However, keep in mind that experiments on several insect orders in hyperoxic conditions have shown that there is no difference in their flight performance (Harrison et al., 2010).

Some authors even suggest that it was the high oxygen levels that allowed the evolution of insect flight in the first place (Graham et al., 1995). In the absence of a good stem-group insect fossil record, I would not add weight behind this hypothesis.

The mechanism behind the oxygen hypothesis’s validity is the way insects breathe, through the tracheal system (Kaiser et al., 2007). The system works almost completely by diffusion, and so as insects gets larger, its efficacy gets smaller, since there is no active process to let the air flow in; this is why large insects are nevertheless still narrow – they need to keep the muscle sites as close to the tracheae as possible. While larger insects have highly-sophisticated tracheal systems aimed at maximising the efficiency of the diffusion, there is a limit set by the exoskeleton – there is only so much space to build these tubes, since connective tissue is also needed. What the Kaiser et al. (2007) study showed was that when the beetles were raised in an atmosphere with higher-than-normal oxygen, the amount of energy invested in expanding the tracheal system decreases, despite attaining the same mass. Specifically, they showed that it’s not overall body size that matters, but the growth of certain body parts: the limiting factor is getting oxygen through all the constrictions and twistings of the tracheal system to the head; see figure above (especially the last line of the caption).

This subsequently means that if they were to expand their tracheal system, they could reach much larger sizes, and this is what happened in the Permian and Carboniferous – the oxygen was there, and so they could afford to reach large sizes without compromising their breathing systems. Today’s largest beetles are at the very limit allowed by current oxygen levels, 16 cm (Kaiser et al., 2007). Another limitation to consider is that the tracheal system can’t get too complicated, or else water balance regulation in the insect gets compromised, since the tracheae interfere with the haemolymph.

Keep in mind that recent research is revealing that insects also have an active breathing system (Socha et al., 2008). However, whether its powerful enough to play a significant role is still under debate.

Of course, if you want to test the effect of oxygen on insect size, it’s very easy to do it experimentally. This has been done with all sorts of insects, and the results are clear for most of them that higher oxygen levels lead to larger insect mass (figure above; Peck & Maddrell, 2005). Better yet, the larger sizes hold up even over multiple generations (Henry & Harrison, 2004), and might even become encoded for in the genome after several generations, regardless of oxygen levels (Klok & Harrison, 2009).

One factor that has been suggested as a limit on insect size even in hyperoxic conditions is exoskeletal growth – they can only grow so much. Lease & Wolf (2010) tested the investment in chitin in insects of all size ranges and found that investment in chitin – i.e. exoskeletal growth – scales isometrically: as the insect grows larger, so does the investment in chitin and growth, meaning this poses no limitation to insect size.

The case for linking oxygen levels and body size is solid and makes a lot of sense, and is currently accepted as the most parsimonious explanation for the giant Palaeozoic arthropods. In fact, it’s been intuitively known for a long time. For example, Rutten (1966) proposed that the Carboniferous had very high oxygen levels, basing his hypothesis not on geochemistry, but on the presence of these giant insects (this was later vindicated by geochemistry). However, there are still niggling uncertainties, mostly owing to imprecisions in palaeo-oxygen level measurements, and the slightly decoupled patterns of oxygen and body size fluctuations in the fossil record (Butterfield, 2009), a problem exacerbated by the patchiness of the fossil record of this time (Labandeira, 2005). These criticisms are valid. Okajima (2008) studied dragonfly size changes through geological time and found no correlation at all with oxygen levels. Either something else was happening in the Carboniferous, or there is some critical morphological/physiological difference between the Odonata and Protodonata that allowed the Protodonata to become gigantic.

Alternative explanations for the giant Palaeozoic insects include evolution of large size as a defence against the newly-evolved insectivorous tetrapods (Shear & Kukalová-Peck, 1990), or even as a result of an arms race (Peck & Munroe, 1999). Also, let’s not forget the driver of the oxygen spikes: primary producers (Berner et al., 2003). The gigantism may just have been a response to an abundance of food.

With all that said, all I can give as a sort of concensus is my own idea. That oxygen affects insect size is fairly obvious from the experimental data. The freak giants of the Carboniferous were just that – freaks. They were unique, and while the higher oxygen levels enabled their gigantism, the oxygen levels weren’t the drivers or the causes of the gigantism. I attribute that to ecology. Whether it was the abundance of food or coevolution, I won’t stick my neck out and say without more data.

Enough about the ancient stuff. It would be a mistake to think that insects don’t undergo gigantism in nature today. After all, the largest insects around are pretty large, withthe aptly-named cerambycid beetle Titanus giganteus reaching up to 20 cm. Other beetles (e.g. Xixuthrus heros, Fiji, see Yanega et al. (2004)) fill out the top 5 of the largest insects, followed by orthopterans and odonates (the 10 cm long, 19 cm wingspan pseudostigmatid damselfly Megaloprepus caerulatus is the largest extant odonate, a condition attributed to both phylogeny and ecology (Groeneveld et al., 2007)). By contrast, mydaid flies, known for being large, “only” reach 5.5 cm.

In New Zealand, the geographic isolation and absence of rodents has led to some unique insect faunas exhibiting large sizes, with some gigantic beetles, orthopterans (weta!), phasmids and ghost moth species being the result (Daugherty et al., 1993). Weta especially have been a center of attention, with the suggestion that they’ve evolved to fill the same ecological space that rodents occupy in continents (Fleming, 1977). It’s worth noting that when mice were artificially introduced to New Zealand, the weta population declined greatly (McIntyre, 2001). Besides weta being the largest (and heaviest: Deinacrida heteracantha, recorded pregnant at 71g, but normally up to 32g) orthopterans, Gryllus alexandri (cricket, small Pacific island) and Thaumatogryllus conanti(tree cricket, Nihoa) are the largest of their subfamilies; the same is true for the Lasiorhynchus barbicornis, the largest ever weevil (New Zealand); Labidura herculeana (8 cm dermapteran, St. Helena) and Pharnacia serratipes (phasmid, Indonesia) are the largest known species in their orders (Chown & Gaston, 2010). These examples provide more evidence for the island rule being applicable to insects. Another aspect of the island rule, in addition to the gigantism, is that flying taxa (birds, insects) will evolve flightlessness, and this is exemplified by the 10 cm flightless Madagascar hissing cockroach, Gromphadorhina portentosa.

Of course, gigantism is a relative term, not an absolute one. In holometabolous insects (i.e. those with a larva-pupa-adult life cycle), final size is determined by the amount of food received in the larval stage. Life history adaptations may cause larvae of one species to gain more food than closely-related species. As an example, take Megaxenusaderid beetles. Aderids are generally pretty small, butmany Megaxenus species are parasitic in termite nests, getting fed by the termites as if they were part of the colony. And it’s true that Megaxenus aderids are the largest of the aderids (Lawrence et al., 1990). A similar phenomenon can be observed in many conopid and pyrgotid flies, whose larvae are parasitic, hatching inside the bodies of large beetles and hymenopterans, eating them inside out; that’s a lot of food, and adult conopids and pyrgotids are pretty large. These can also be seen as gigantisms.

One parasite has taken advantage of this fact of insect physiology. The microsporidianNosema whitei parasitisesthe larval red flour beetle, Tribolium castaneum, and forces it to remain in the larval stage, when the larva can keep growing (Onstad & Maddox, 1990); in other words, the parasite induces gigantism in it, and kills it before pupation (Bass & Armstrong, 1992). This favours the parasite’s transmission (Forbes, 1993).